Elevated glucocorticoid concentrations during gestation predict reduced reproductive success in subordinate female banded mongooses

Abstract

Dominant females in social species have been hypothesized to reduce the reproductive success of their subordinates by inducing elevated circulating glucocorticoid (GC) concentrations. However, this ‘stress-related suppression' hypothesis has received little support in cooperatively breeding species, despite evident reproductive skews among females. We tested this hypothesis in the banded mongoose (Mungos mungo), a cooperative mammal in which multiple females conceive and carry to term in each communal breeding attempt. As predicted, lower ranked females had lower reproductive success, even among females that carried to term. While there were no rank-related differences in faecal glucocorticoid (fGC) concentrations prior to gestation or in the first trimester, lower ranked females had significantly higher fGC concentrations than higher ranked females in the second and third trimesters. Finally, females with higher fGC concentrations during the third trimester lost a greater proportion of their gestated young prior to their emergence from the burrow. Together, our results are consistent with a role for rank-related maternal stress in generating reproductive skew among females in this cooperative breeder. While studies of reproductive skew frequently consider the possibility that rank-related stress reduces the conception rates of subordinates, our findings highlight the possibility of detrimental effects on reproductive outcomes even after pregnancies have become established.

The influence of stress hormones and aggression on cooperative behaviour in subordinate meerkats

“…In some species, dominant individuals direct aggression towards subordinates, raising their glucocorticoid concentrations (GCs: [4][5][6][7]. The elevation of GCs in subordinates can suppress their reproductive activity (4)(5)(6)8) allowing dominants to monopolize reproductive opportunities (6). However, such changes in subordinate GCs could also carry additional benefits or costs for dominants by increasing or decreasing subordinate cooperative behaviour, respectively (9)(10)(11)(12)(13)(14)(15)(16).…”

Effect of food limitation and reproductive activity on fecal glucocorticoid metabolite levels in banded mongooses

“…Thus, only the energy mobilization hypothesis (glucocorticoid production should increase when energetic demands or deficits are greatest) and behavior hypothesis (glucocorticoid production should decrease during the breeding season) [31] are plausible explanations for seasonality in glucocorticoid production in banded mongooses. If anything, our study population and banded mongooses in Uganda [43,50] exhibit increases in glucocorticoid production during the breeding season, not decreases. Given that the breeding season increases associated with provisioning pups and subordinate female pregnancies may ultimately be driven by energetic losses in the adult carers and subordinate females [43,50], and our observation that breeding season peaks are unimodal i.e.…”

“…Groups with dispersed and more abundant anthropogenic provisioning, had lower fGCM peaks, delayed until late dry season, coinciding with first parturition. Portions of these fGCM peaks may be explained by late pregnancy fGCM increases in subordinate females [50] or by fGCM increases associated with provisioning of pups [43]. However, these peaks were not repeated in subsequent parturition events later in the breeding season.…”

“…Alloparental care is associated with increased fGCMs in banded mongoose, although this may be driven by energetics [43]. Lower ranked female banded mongooses have higher fGCMs later in pregnancy, although this may also be driven by energetic differences during gestation, specifically, exclusion of subordinates from food resources by higher ranked females [50].…”

“…(a) GCs increase in female meerkats (Suricata suricatta) as pregnancy progresses [8] (b) GCs increase in mate-guarding male long-tailed macaques (Macaca fascicularis) [69] (c) Mating, parturition, associated agonistic encounters, and pup depredations increase GCs in captive banded mongooses [38] (d) Alloparental care (pup provisioning) in banded mongoose is associated with increased fGCMs (although this may be driven by energetic losses) [43] (e) Subordinate female banded mongoose have higher fGCM concentrations in late pregnancy than higher ranked females (although this may be driven by exclusion from food resources and resulting energetic losses) [50] C. Predation risk…”